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Molecular Characteristics of Carnivore Protoparvovirus 1 with High Sequence Similarity Between Wild and Domestic Carnivores in Taiwan

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Molecular Characteristics of Carnivore Protoparvovirus 1 with High Sequence Similarity Between Wild and Domestic Carnivores in Taiwan pathogens Article Molecular Characteristics of Carnivore protoparvovirus 1 with High Sequence Similarity between Wild and Domestic Carnivores in Taiwan Ai-Mei Chang 1,2 and Chen-Chih Chen 2,3,4,* 1 International Program in Animal Vaccine Technology, International College, National Pingtung University of Science and Technology, Pingtung 91201, Taiwan; [email protected] 2 Research Center for Animal Biologics, National Pingtung University of Science and Technology, Pingtung 91201, Taiwan 3 Institute of Wildlife Conservation, College of Veterinary Medicine, National Pingtung University of Science and Technology, Pingtung 91201, Taiwan 4 Department of Veterinary Medicine, College of Veterinary Medicine, National Pingtung University of Science and Technology, Pingtung 91201, Taiwan * Correspondence: [email protected]; Tel.: +886-87703202 (ext. 6596) Abstract: Carnivore protoparvovirus 1 (CPPV-1) is a DNA virus causing gastrointestinal disease and immunosuppression in various terrestrial carnivores. Domestic dogs and cats are considered the primary CPPV-1 reservoirs. The habitat overlap of wild carnivores and free-roaming dogs increases the threat of CPPV-1 transmission between them. This study explored the CPPV-1 distribution among wild carnivores in Taiwan through PCR screening and compared the partial capsid protein (VP2) gene sequences from wild and domestic carnivores. In total, 181 samples were collected from 32 masked palm civets (Paguma larvata), 63 Chinese ferret badgers (Melogale moschata), and 86 crab-eating mongooses (Herpestes urva), from 2015 to 2019 were screened for CPPV-1. The average Citation: Chang, A.-M.; Chen, C.-C. prevalence of CPPV-1 was 17.7% (32/181), with the highest prevalence in masked palm civets (37.5%). Molecular Characteristics of Carnivore protoparvovirus 1 with High Sequence In addition, a masked palm civet was coinfected with two CPPV-1 strains. Among the 33 partial Similarity between Wild and VP2 gene sequences, 23 were identical to the sequences amplified from domestic dogs and cats in Domestic Carnivores in Taiwan. Asia, and the remaining 10 were identified for the first time. This study supported the circulation of Pathogens 2021, 10, 671. https:// CPPV-1 strains with the same genomic features as domestic carnivores that are also in wild carnivores doi.org/10.3390/pathogens10060671 from the same environment in Taiwan by molecular data. Therefore, further population control and health management of free-roaming domestic carnivores are recommended. Academic Editor: Anna Honko Keywords: Carnivore protoparvovirus 1; wild carnivores; domestic carnivore; virus transmission; Taiwan Received: 20 April 2021 Accepted: 26 May 2021 Published: 29 May 2021 1. Introduction Publisher’s Note: MDPI stays neutral Domestic dogs (Canis familiaris) and cats (Felis catus) are the most abundant carnivores with regard to jurisdictional claims in published maps and institutional affil- worldwide [1,2]. They are abundant in human settlements and are considered invasive iations. species in natural environments outside these settlements. An increasing number of domestic dogs and cats can disturb and potentially threaten native fauna through predation, habitat competition, and disease transmission [3]. Considering the close phylogenetic relationship between wild and domestic carnivores, some pathogens infecting domestic carnivores may be transmitted to wild carnivores, causing disease and ultimately population decline in Copyright: © 2021 by the authors. wild carnivores. For instance, rabies virus [4], canine distemper virus (CDV) [5], Carnivore Licensee MDPI, Basel, Switzerland. protoparvovirus 1 (CPPV-1) [6,7], feline immunodeficiency virus (FIV), and feline leukemia This article is an open access article distributed under the terms and virus (FeLV) [8], have been reported to be transmitted between wild and domestic carnivores; conditions of the Creative Commons this transmission can ultimately affect the population of endemic carnivores. Attribution (CC BY) license (https:// CPPV-1 is a highly contagious pathogen belonging to the family Parvoviridae [9,10]. creativecommons.org/licenses/by/ Various CPPV-1 variants have been identified, such as feline panleukopenia virus (FPV); 4.0/). canine parvovirus (CPV-2), along with its various antigenic variants CPV-2a, CPV-2b, and Pathogens 2021, 10, 671. https://doi.org/10.3390/pathogens10060671 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, 671 2 of 14 CPV-2c [11]; mink enteritis virus (MEV); blue fox parvovirus (BFPV); raccoon parvovirus (RPV); and raccoon dog parvovirus (RDPV) [12]. CPPV-1 is a single-stranded DNA virus, and its gene structure consists of two major open reading frames (ORFs), encoding for nonstructural proteins (NS1 and NS2), and capsid proteins (VP1 and VP2) [13]. Domestic carnivores are considered to be the primary reservoirs of CPPV-1 [14]. A survey in South Korea revealed a CPV-2a seroprevalence of 93.8% in the stray dog population [15]. DiGangi et al. [16] screened feral cats for CPPV-1 within 24 h of their arrival at a shelter and identified a feline parvovirus prevalence of 39.8%. Apart from domestic animals, various hosts in the order Carnivora have been identified as having CPPV-1 infection [17]. CPPV-1 can infect more than 280 species of Carnivora and can cause a high degree of host strain-specific infection in different carnivores [18,19]. CPV-2 variants have been reported to induce hemorrhagic enteritis, gastroenteritis, and myocarditis in domestic dogs. In addition, CPV-2c has been indicated to induce more severe clinical manifestations than CPV-2a and -2b can [11,20,21]. CPPV-1 infection has been evidenced to reduce the survival rate of wolf (Canis lupus) pups [12–14]. Creel et al. [22] found that CPPV-1 infection contributes to the high annual mortality rate of African wild dogs (Lycaon pictus). Contact with domestic dogs was the primary risk factor for CPPV-1 infection in African wild dogs [14]. The Chinese ferret badger (Melogale moschata), masked palm civet (Paguma larvata), and crab-eating mongoose (Herpestes urva ) are endemic carnivores commonly found in rural areas of Taiwan [23]. However, due to human encroachment into their original habitats, an abundance of free-roaming dogs in the rural areas of Taiwan has been recorded [24]. The sympatric distribution of wild and domestic carnivores may increase the risk of pathogen transmission. Therefore, pathogen surveillance of wild carnivores that enter rural areas is necessary for wildlife conservation and disease control planning [25]. CPV-2a, -2b, -2c, and FPV infections have been reported in domestic carnivores and free-roaming leopard cats in Taiwan, with CPV-2c becoming a dominant variant after 2017 [25–27]. However, the distribution of CPPV-1 in other wild carnivores in Taiwan remains unclear. The primary objective of this study was to investigate the distribution of CPPV-1 and characterize the present CPPV-1 variants contributing to infection in Taiwanese wild carnivores. We collected samples from animals captured in live traps and from dead individuals to screen for CPPV-1 infection. Molecular screening for CPPV-1 was conducted by a PCR assay targeting the partial VP2 gene region. The positive amplicons were sequenced, and molecular phylogenetic analysis was performed to compare the relationships of amplified CPPV-1 between domestic and wild carnivores. 2. Results 2.1. Prevalence of CPPV-1 in the Wild Carnivore Population Our study was conducted in Taiwan from 2015 to 2019. We collected 118 live-trapped (LT) wild carnivore samples from 6 masked palm civets, 32 Chinese ferret badgers, and 80 crab-eating mongooses. There were 63 found-dead (FD) wild carnivore samples from 26 masked palm civets, 31 Chinese ferret badgers, and 6 crab-eating mongooses (Table1). The overall prevalence of CPPV-1 in the samples from wild carnivores was 17.7% [32/181, 95% confidence interval (CI): 12.2–23.2%], of which 10.2% accounted for LT individuals (12/118) and 31.7% accounted for FD individuals (20/63). The CPPV-1 prevalence was significantly higher in FD individuals than in LT individuals (chi-squared test; p < 0.001). CPPV-1 infection was detected in all tested species; the highest prevalence was 37.5% [12/32, 95% confidence interval (CI): 20.73–54.27%] of CPPV-1 observed in masked palm civets. The prevalence in adult, juvenile, male, and female wild carnivores was 17.1% (22/129, 95% CI: 10.6–23.5%), 16.7% (6/36, 95% CI: 4.5–28.8%), 21.2% (18/85, 95% CI: 12.5–29.9%), and 15.0% (12/80, 95% CI: 7.2–22.8%), respectively. No significant difference in CPPV-1 detection was found for age (chi-squared test; p = 0.844) or sex (chi-squared test; p = 0.409; Table2). Pathogens 2021, 10, 671 3 of 14 Table 1. Species, age, and sex of wild carnivores screened for Carnivore protoparvovirus 1 in Taiwan, 2015–2019. Age Sex Family, Species Common Name Sample Type Total Adult Subadult Juvenile ND 1 Female Male ND 1 Herpestidae, Crab-eating LT 2 53 25 0 2 43 36 1 80 Herpestes urva mongoose FD 3 5 0 1 0 1 2 1 6 Mustelidae, Chinese ferret LT 25 5 0 2 11 18 3 32 Melogale moschata badger FD 29 1 0 1 15 16 0 31 LT 4 1 0 1 2 3 1 6 Viverridae, Masked palm civet Paguma larvata FD 13 4 0 9 8 10 8 26 1 ND = no data. 2 LT = live trapped. 3 FD = found dead. Table 2. Prevalence and variants of Carnivore protoparvovirus 1 infection in wild carnivore samples. Sample 95% CI Variants Species No. No. Prevalence Type Individuals Positive Lower Upper FPV CPV-2a CPV-2b CPV-2c LT 1 80 4 5.0% 0.2% 9.8% 2 0 0 2 Crab-eating 2 mongoose FD 6 1 16.7% 0.0% 46.5% 0 0 0 1 Sum 86 5 5.8% 0.9% 10.8% LT 6 1 16.7% 0.0% 46.5% 0 0 0 1 Masked 3 palm civet FD 26 11 42.3% 23.3% 61.3% 1 5 1 5 Sum 32 12 37.5% 20.7% 54.3% Chinese LT 32 7 21.9% 0.2% 9.8% 1 4 0 1 ferret FD 31 8 25.8% 10.4% 41.2% 0 5 0 3 badger Sum 63 15 23.8% 13.3% 34.3% Total 181 32 17.7% 12.1% 23.2% 4 15 1 13 1 LT = live trapped.
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